The traditional motion coherence paradigm cannot distinguishbetweenlocalandgloballimitstomotion per-ception and has hence obscured our understanding of whatlimitsglobalmotionprocessingdu
Trang 1jo u rn al h om ep age : ht t p : / / w w w e l s e v i e r c o m / l o c a t e / d c n
Catherine Manninga,∗, Steven C Dakinb,c, Marc S Tibberb, Elizabeth Pellicanoa
a Centre for Research in Autism and Education (CRAE), Institute of Education, University of London, 55-59 Gordon Square,
Institute of Education, London WC1H 0NU, UK
b UCL Institute of Ophthalmology, University College London, Bath Street, London EC 1V9, UK
c NIHR Biomedical Research Centre at Moorfields Eye Hospital, 162 City Road, London EC 1V 2PD, UK
a r t i c l e i n f o
Article history:
Received 5 February 2014
Received in revised form 16 July 2014
Accepted 18 July 2014
Available online 1 August 2014
Keywords:
Visual development
Motion processing
Direction discrimination
a b s t r a c t
Thedevelopmentofmotionprocessingisacriticalpartofvisualdevelopment,allowing childrentointeractwithmovingobjectsandnavigatewithinadynamicenvironment How-ever,globalmotionprocessing,whichrequirespoolingmotioninformationacrossspace, developslate,reachingadult-likelevelsonlybymid-to-latechildhood.Thereasons under-lyingthisprotracteddevelopmentarenotyetfullyunderstood.Inthisstudy,wesoughtto determinewhetherthedevelopmentofmotioncoherencesensitivityislimitedbyinternal noise(i.e.,imprecisioninestimatingthedirectionsofindividualelements)and/orglobal poolingacrosslocalestimates.Tothisend,wepresentedequivalentnoisedirection dis-criminationtasksandmotioncoherencetasksatbothslow(1.5◦/s)andfast(6◦/s)speeds
tochildrenaged5,7,9and11years,andadults.Weshowthat,aschildrengetolder,their levelsofinternalnoisereduce,andtheyareabletoaverageacrossmorelocalmotion esti-mates.Regressionanalysesindicated,however,thatage-relatedimprovementsincoherent motionperceptionaredrivensolelybyimprovementsinaveragingandnotbyreductions
ininternalnoise.Ourresultssuggestthatthedevelopmentofcoherentmotionsensitivity
isprimarilylimitedbydevelopmentalchangeswithinbrainregionsinvolvedinintegrating motionsignals(e.g.,MT/V5)
©2014TheAuthors.PublishedbyElsevierLtd.ThisisanopenaccessarticleundertheCC
BYlicense(http://creativecommons.org/licenses/by/3.0/)
The processing of motion is a critical partof visual
development,allowingchildren totrackmoving objects
withtheireyes, toreachfor and graspobjects thatare
in motion, and to navigate within a dynamic world
Motionprocessing contributestoa range ofelementary
visualfunctionsincludingthesegmentationofscenesinto
differentobjects and surfaces, the perception of depth,
∗ Corresponding author Tel.: +44 207 331 5135.
E-mail address: c.manning@ioe.ac.uk (C Manning).
the registration of trajectories and the identification of objects.Often,it isimportant tocombinemotion infor-mationacrossspace,for exampleinorder todetermine theoveralldirectionofaflockofbirds,eachofwhichwill
befollowinga differentmotiontrajectory.Thisability– termed global motion processing – is typically tested experimentally using the motion coherence paradigm (Newsome and Paré, 1988), which requires observers
tojudgethedirectionof coherentlymoving dotsinthe presenceofrandomlymovingnoisedots
Given theimportanceof motionprocessing invisual development,itisperhapsunsurprisingthatsomeaspects
ofmotionprocessing(e.g.,directionalselectivity)develop
http://dx.doi.org/10.1016/j.dcn.2014.07.004
1878-9293/© 2014 The Authors Published by Elsevier Ltd This is an open access article under the CC BY license ( http://creativecommons.org/
Trang 2early in life (Wattam-Bell, 1991, 1992; see Braddick
et al.,2003,for review).However,othertypes ofvisual
motionprocessingfollowaprotracteddevelopmentand
only reach adult-like levels by mid-to-late childhood
For example, the minimum speed required to support
perception of motion-defined form and the maximum
displacementsupportingperceptionofmovementmature
byaround7–8years(Haywardetal.,2011;Parrishetal.,
2005), motion coherence thresholds reach adult-like
levelsbetween10and14years(Gunnetal.,2002;Hadad
etal.,2011)andspeeddiscriminationabilitiesarenotyet
fullyadult-likeby11years(Manningetal.,2012).Such
motionprocessing abilities rely primarilyonthe dorsal
pathway (Milner and Goodale, 1995), which originates
frommotion-sensitiveneuronsinareaV1,andprojectsto
extrastriateareasincludingMT/V5.WhileneuronsinV1
cansignalthepresenceoflocalmotion(HubelandWiesel,
1962), neuronsin V5 play a key role in global motion
processing,astheyhavelargerreceptivefieldscapableof
integratinginputsfromV1(Mikamietal.,1986)
Adultstudiesofvisualmotionprocessingsuggestthe
existence of atleast two distinct systems tunedto
dif-ferentrangesofspeed(Burretal.,1998;Edwardsetal.,
1998;Thompsonetal.,2006;alsoseereviewbyBurrand
Thompson, 2011), which may follow different
develop-mentaltrajectoriesinthematuringbrain.Haywardetal
(2011)reportedgreaterimmaturityinsensitivityto
coher-entmotionattheslowestspeedtested(0.1◦/s)compared
to faster speeds of 0.9 and 5◦/s Also, in a speed
dis-criminationtask,Manningetal.(2012)reporteda more
gradualdevelopmentofthresholdsforslow(1.5◦/s)than
fast(6◦/s)speeds.However,Hadadetal.(2011)didnot
finddifferentratesofdevelopmentformotioncoherence
thresholdsmeasuredwithrandomdotstimulimovingat
4◦/sand18◦/s.Together,thisresearchsuggeststhatmotion
processing forintermediate and fastspeedsmay follow
similarratesofdevelopment,butthatprocessingofmuch
slower speeds (e.g., 0.1 and 1.5◦/s) may develop more
slowly
Globalmotionprocessingabilitiesinchildhoodare
gen-erallythoughttobelimited bypoorintegrationoflocal
motioncuesoverspace(e.g.,Ahmedetal.,2005;Hadad
et al., 2011; Manning et al., 2012) Such integration is
believed to occur in higher-order areas of the motion
processing hierarchy, suchas in area MT/V5 (Born and
Tootell,1992;Brittenetal.,1992).Yetperformanceontasks
traditionallyusedtoassessglobalmotionprocessing(i.e.,
motioncoherenceparadigms;NewsomeandParé,1988)
isnotlimitedsolelybyglobalintegration.Suchtasksare
likelylimitednotonlybyanobserver’sabilitytoglobally
poolthemotionofindividualdotsacrossspace,butalsoby
theirabilitytoestimatethelocalmotiondirectionofeach
dot(BarlowandTripathy,1997),andbytheirabilityto
seg-mentthesignaldotsfromthemaskingnoise(Dakinetal.,
2005;Tibberetal.,2014;Websteretal.,2011)
Increasedneuralvariabilitywouldleadtoimprecisionin
estimatingindividualdotdirections,which,whenpooled,
couldleadtoelevatedmotioncoherencethresholds.This
neural variability has been termed‘internal noise’, and
hasmanypotentialsources,includingphotonnoise,
vari-ability in the firingof action potentials, and variability
in synaptic transmission (Faisal et al., 2008) Through development,neuronsinareaV1undergoextensive synap-tic pruning(Gareyand de Courten, 1983; Huttenlocher
etal.,1982;HuttenlocheranddeCourten,1987),andthe bandwidthsofdirection-selectivecellsreducewithage(at leastintheprimatebrain,Hattaetal.,1998).Itis possi-blethatsuchdevelopmentalchangesmightbemanifestas reducedinternalnoisewithage
The traditional motion coherence paradigm cannot distinguishbetweenlocalandgloballimitstomotion per-ception and has hence obscured our understanding of whatlimitsglobalmotionprocessingduringdevelopment (andinavarietyofneurodevelopmentaldisorders;Dakin andFrith,2005).Toaddressthisissue,thecurrentstudy usedtheequivalentnoiseparadigm(Barlow,1956;Pelli,
1990)to determine whether local or global processing limitsmotioncoherencesensitivityindevelopment.The equivalentnoiseparadigmisbasedoncomparinghuman performancetothat ofanidealobserverthat islimited bothbyadditiveinternalnoiseandbyhowcompletelyit samplestheinformationavailablefromthestimulus(Pelli,
1990).Whenequivalentnoiseanalysisisappliedto direc-tiondiscrimination(Dakinetal.,2005),internalnoisemaps onto theprecisionwithwhich individual motion direc-tionsareestimatedand samplingrepresentsanestimate
of the effectivenumber of local motiondirections that aregloballypooled(oraveraged).Whereasmotion coher-encestimulicontainbothsignaldotsandrandomlymoving noise dots,equivalentnoise stimuli containdotswhose directions (onany one trial)are sampledfrom a single Gaussian distribution(Dakinet al., 2005).The standard deviationofthis distributionisvariedacrossconditions,
inordertomanipulatethelevelofstimulusvariability(or
‘externalnoise’;seeFig.1A)
Intheequivalentnoisetask,theobserverisaskedto dis-criminatethemeandirectionofdots,andtheperformance measureisthesmallestdifferenceindirectionfromafixed referencedirection(e.g.,upwards)thatobserverscan reli-ablyreport.Withnodirectionalvariance (i.e.,whenthe standarddeviationis0◦andallelementsmoveinthesame direction),theobserver’sperformanceislimitedbothby internalnoiseandsampling.Consequently,smallamounts
ofextraexternalnoisehavelittleeffectonthresholds,as
itisswampedbytheobserver’sowninternalnoise How-ever,asthelevel ofexternal noise isincreased,a point
is reachedwhere theexternal noise exceeds the inter-nalnoiseinherentinthesystem,andthresholdsstartto increase withtheadditionoffurtherexternal noise An equivalentnoisefunctioncanbefittothesedatatoderive estimatesoftheindividual’sinternalnoiseandsampling (seeFig.1A)
Asthresholdsaremeasuredacrossarangeofexternal noiselevels,theequivalentnoisemethodtypicallyrequires severalthousandtrials,makingit unsuitablefor investi-gatingthevisualabilitiesofchildren,whomaygetbored andbecomeinattentive.However,amoreefficient equiv-alentnoiseprocedurehasbeendeveloped,whichprovides reliableestimatesofinternalnoiseandsamplinginfewer than100trials(Tibberetal.,2014).Inthisnovelmethod, twohighlyinformativepointsontheequivalentnoise func-tionareprobed(seegreyline,Fig.1B).Inonecondition
Trang 3Fig 1. (A) Equivalent noise functions relating direction discrimination thresholds to the standard deviation of dot directions (i.e., external noise) Lower sampling is represented by an equivalent noise function that is shifted vertically upwards, whilst higher levels of internal noise require more external noise
to be added before thresholds increase (B) The black circles and curve represent the standard equivalent noise paradigm where direction discrimination thresholds are measured at multiple levels of external noise Large standard deviations of dot directions reflect high external noise in the stimulus The grey circles and curve are derived using a rapid version of the equivalent noise paradigm, which measures performance at two maximally informative noise levels In the ‘no noise’ condition, there is no external noise (i.e., the standard deviation of dot directions is 0 ◦ ) and the threshold is taken as the finest direction discrimination possible In the ‘high noise’ condition, we measure the maximum noise that can be tolerated when the observer is judging if the pattern is moving either +45◦or −45 ◦ of vertical (C) Example of a stimulus in the ‘low noise’ condition, where the mean direction of dots is +4◦, and the standard deviation of directions is 0◦ (D) Example of a stimulus in the ‘high noise’ condition, where the mean direction of dots is +45◦, and the standard deviation of dot directions is 45 ◦ Arrows are provided for illustrative purposes only, to represent the direction of motion.
(‘nonoise’, Fig.1C),thestandard deviationofdot
direc-tionsis0◦,andanadaptivestaircaseprocedureisusedto
estimatethefinestdirectiondiscriminationpossible.Inthe
othercondition(‘highnoise’,Fig.1D),anadaptivestaircase
procedureestimateshowmuchdirectionalvariabilitycan
betoleratedwhilediscriminatingalarge(±45◦)directional
offset.Asthesethresholdshaveconfidenceintervalsthatlie
inorthogonalplanes,thefitoftheequivalentnoise
func-tionisefficientlyconstrainedtoprovidereliableestimates
ofinternalnoiseandsampling
Here,weusedTibberetal.’srapidversionofthe
equiv-alent noise direction integration paradigm alongside a
traditionalmotioncoherencetasktoinvestigatethe
fac-torslimitingthedevelopmentofglobalmotionprocessing
Thesemethodsallowedustoinvestigate(1)how
inter-nal noise and sampling develop, and (2) the extent to
whichchangesinthesefactorsimpactuponacommonly
usedmeasureofglobalmotionprocessing,namelymotion
coherencethresholds Due to the possibility of distinct
developmentaltrajectoriesfordifferentspeeds(Hayward
etal.,2011;Manningetal.,2012),equivalentnoiseand
motioncoherencetaskswerepresentedattwostimulus
speeds:slow(1.5◦/s)andfast(6◦/s)
Itiscommonlyassumedthatmotioncoherence
thresh-olds are limited by poor integration of local motion
information(e.g.,Hadadetal.,2011).Wetherefore
hypo-thesised that sampling would increase with age and
that this would contribute to age-related reductions in motioncoherencethresholds.Derivinghypothesesabout thedevelopmentofinternalnoisewaslessstraightforward Indeed,someresearchershavenotedthatchildren have hightrial-to-trialbehaviouralvariabilitywhichdecreases with age (e.g., Williams et al., 2005), where higher behavioural variability isthoughtto reflect higher neu-ronalvariability(i.e.,noise;Foxetal.,2007,butseealso
Beck et al., 2012) Additionally, Skoczenski and Norcia (1998)measuredinternalnoiseininfantsusingan equiv-alentnoisetechniquewithvisuallyevokedpotential(VEP) responsesandreportedthathighlevelsofinternalnoise
ininfancylimitedcontrastsensitivity.Similarly,Bussetal (2006)demonstratedincreasedlevelsofinternalnoisein childrenaged5–10yearscomparedtoadults,withchildren beinglesssusceptibletotheeffectsofexternalnoise (rov-ingintensities)inanauditoryintensitydiscriminationtask Alternatively,somehavesuggestedthatneuronal variabil-ityin factincreaseswithagefrom8years toadulthood,
as measured by trial-by-trial EEG variability (McIntosh
etal.,2008).Evidently,internalnoisehasbeenmeasured
in arange ofdifferentways andit isnot yetclearhow thesemeasuresrelatetoeachother.Inthecurrentstudy,
wethereforeaimedtoinvestigatehowinternalnoiseand samplingchangethroughchildhoodforadirection integra-tiontaskandtodeterminewhethersuchchangeslimitthe developmentofmotioncoherenceperception
Trang 42 Materials and methods
2.1 Participants
Fivegroupsofparticipantsweretested,with21
5-year-olds(M=5years;4months,range4;10–5;10,14females),
277-year-olds(M=7years;3months,range6;7–7;10,
11females),259-year-olds(M=9years;2months,range
8;8–9;9, 11females),20 11-year-olds (M=11 years;3
months, range 10; 8–11; 9, 14 females) and 30 adults
(M=26years;9months,range21;5–35;10,15females)
includedinthefinaldataset.Childrenwererecruitedfrom
schoolsintheSouthEastofEngland.Normalor
corrected-to-normalvisualacuitywasconfirmedbybinoculartesting
withletteracuitytestsusingopticalcorrectionswhere
nec-essary.Normalacuity wasdefined asa binocularacuity
of6/9orbetterfor5-and7-year-olds(becauseacuityis
stillmaturinginthisagerange;AdamsandCourage,2002;
Ellembergetal.,1999)and6/6orbetterfor9-and
11-year-oldsandadults
Anadditionalnine5-year-oldswereexcludedfromthe
dataset,with onechild failing to passthe visualacuity
screening,onefailingtoreachcriterion(seeSection2.3.1),
three not performing significantly above chance in the
catchtrials(seeSection2.6.2)andfourobtainingmotion
coherencethresholdsabove100%,indicatinganinability
toperformthetask.Oneadditional7-year-oldcouldnot
completethemotioncoherencetask.Anadditionaltwo
9-year-olds,one11-year-oldandoneadultwereexcluded
fromthedatasetduetodiagnosesofdevelopmental
con-ditions
2.2 Apparatusandstimuli
ThestimuliwerepresentedusingMATLAB(The
Math-worksLtd.)usingelementsofthePsychophysicsToolbox
software(Brainard,1997;Kleineretal.,2007;Pelli,1997)
Stimuli were displayed on a Dell Precision M4600
lap-top at a frame rate of 60Hz and a pixel resolution of
1366×768
A yellow-bordered circular aperture (diameter=15◦) andanchor-shapedfixationpoint(0.57×0.57◦)were pre-sented against a grey background witha luminance of
30cd/m2(seeFig.2).Twosmalleryellow-bordered circu-larapertures(diameter=6.12◦)werepresentedtotheleft andrightofthis,servingasreferencepointsforthe repor-tingofmotiondirection.Intheequivalentnoisetask,the leftandrightapertureswerepresentedinthetopcorners
ofthescreenandcontainedimagesofredandgreenreefs, respectively(seeFig.2A).Inthemotioncoherencetask,the leftandrightapertureswerepresentedhalfwaydownthe screen,containingimagesofredandgreenrocks, respec-tively(seeFig.2B)
Thestimuliwerecomprisedof100randomlypositioned white dots(58.7cd/m2), each with a diameterof 0.44◦, driftingfor400mswithinthecentralaperture.Dot pos-itionswereupdatedevery3frameswithdisplacementsof 0.075◦ and0.3◦intheslow(1.5◦/s)andfast(6◦/s) condi-tions,respectively.Dotswereallowedtooverlapandwere notlimitedintheirlifetime
2.3 Procedure Participantscompletedanequivalentnoisetaskanda motioncoherencetaskineach oftwospeedconditions: slow(1.5◦/s)andfast(6◦/s).Intheequivalentnoisetask, dotdirections wererandomlysampledfroma wrapped normaldistributionwitha specifiedmeanandstandard deviation.Theequivalentnoisetaskconsistedoftwo inter-leavedconditionsthatprobedtwoinformativepointson theequivalentnoisefunction toconstrainthefitof the model(seeFig.1B).Inthe‘nonoise’condition,thestandard deviationof dotdirections wasfixedat0◦ (i.e.,alldots movedinthesamedirection),whilethemeandirection
ofthedotswasvaried(leftwardorrightwardofvertical)
tofindthefinestdirectionthatcouldbediscriminated84%
ofthetimeintheabsenceofstimulusnoise (correspond-ingtothemeanplusonestandarddeviationinacumulative normaldistribution).Inthe‘highnoise’condition,themean directionofdotswasfixedat45◦leftwardsorrightwards
Fig 2.Schematic representation of stimuli presented in the ‘high noise’ condition of the equivalent noise task (A) and the motion coherence task (B) The
Trang 5dotdirectionswasvariedtofindthemaximumlevelof
noisethatcouldbetoleratedwhilstidentifyingthesignal
directionwith84%accuracy
Theequivalentnoisetaskwaspresentedas“TheHungry
FishGame”.Participantsjudgedwhetherashoalof“fish”
was“swimming”towardsthered(left)orgreen(right)reef
tofindtheirfood.Childrenweretoldthatsometimesthe
fishallmovedinthesamedirection(‘nonoise’)and
some-timesthefishmovedindifferentdirections(‘highnoise’),in
whichcasetheyhadtodeterminetheoverall(i.e.,average)
direction.Toaidmotivation,childrenweretoldthatthey
werecompetingagainstacartooncharacter,“ScubaSam”
In the motion coherence task, a proportion of dots
movedcoherently in asingle direction(90◦ leftwardor
rightwardofvertical)whiletheremainingdotsmovedin
randomdirections.Thetaskwaspresentedwithinthe
con-textof“TheSharkAttackGame”.Participantswereaskedto
judgewhethertheshoalof“fish”was“swimming”towards
thered(left)orgreen(right)rockstohidefromthe“shark”
Childrenweretoldthatthe“fish” sometimes“panicked”
whentheysawthe“shark”,causingthemtogoindifferent
directions.Toenhancemotivation,childrenweretoldthat
theywerecompetingagainstthe“shark”
Each equivalent noise and motion coherence task
consistedofthreelevels:acombineddemonstrationand
criterionphase(‘level1’),apracticephase(‘level2’),anda
thresholdestimationphase(‘level3’).Inalllevelsinboth
tasks,direction(leftwardorrightwardofvertical)was
ran-domisedoneachtrial
2.3.1 Demonstrationandcriterionphase
Theexperimenterexplainedeachtasktoparticipants
withinthe context of four demonstrationtrials, two of
which were designed to be ‘easy’, and two of which
were‘slightly harder’.In theequivalentnoise task, two
of thetrials demonstrated the ‘no noise’ condition,and
two demonstrated the‘high noise’ condition.Next,
par-ticipantswere presented withup to 20 criterion trials
Intheequivalentnoisetask,‘nonoise’ stimuliwere
pre-sentedwitha directionof 45◦ leftwardorrightward of
vertical.Inthemotioncoherencetask,dotsmovedwith
100%coherence90◦leftwardorrightwardofvertical
Par-ticipantswhofailedtoreachacriterionoffourconsecutive
correctresponseswithin20trialsweregivenashort
ver-sionofthetaskandexcludedfromanalysis(n=1).Children
respondedeitherverballyorbypointing,withthe
experi-menterrelayingtheresponsetothecomputer.Visualand
verbalfeedbackandencouragementwereprovided
2.3.2 Practicephase
Eightpracticetrialswerepresentedinafixedorderfor
eachtaskwithincreasingdifficulty.Intheequivalentnoise
task,four‘nonoise’stimuliandfour‘highnoise’stimuliwere
presentedinalternatingorder.Participantsreceived
feed-backasbefore,buttherewasnocriterionforproceedingto
thenextphase
2.3.3 Thresholdestimationphase
Boththeequivalentnoiseandmotioncoherencetasks
employedtheQUESTadaptivestaircasemethod(Watson
and Pelli,1983).Intheequivalentnoisetask, two stair-cases(75trialseach)wereinterleavedforeachofthe‘no noise’and‘highnoise’conditions.Inthe‘nonoise’ condi-tion,theQUESTfunctiontrackedthebasicdirectionoffset thresholdintheabsenceofnoise.Inthe‘highnoise’ condi-tion,themeandirectionofmotionwassetto±45◦ and
QUEST tracked the maximum level of noise that could
be tolerated whilst discriminating the mean direction
Anadditional15catchtrialswereinterleavedrandomly, presenting stimuli identical to those used in the crite-rionphase.Thisyielded165trialsintotalforeachspeed condition
Inthemotioncoherencetask,asingleQUESTstaircase
of75trialstrackedtheminimumcoherencelevelrequired foraccurate(84%correct)directiondiscrimination.Asin the equivalent noise task, there were an additional 15 catch trials, which presented stimuli used in the crite-rion phase This resulted in 90 trials in total for each speed condition.Trials weredivided intofourblocks of equal lengthfor each conditionof eachtask Whenthe end of a blockwasreached, participantswereshown a simulated graph of the “points” they and their “oppo-nent”(“ScubaSam” or the“shark”)had attained These pointswererandomlyjitteredaroundafixedsetofvalues
tominimiserewardandmotivationeffects onthreshold estimates
2.4 Eyetracking
Toestablishwhetherdevelopmentaldifferencesintask performancecouldbeaccountedforbydifferencesin abil-itytomaintainfixation,weusedaTobiiX2-30Compact eyetrackermountedontothescreentocollectfixationdata forasubsetofparticipants,including12five-year-olds,17 seven-year-olds,11nine-year-olds,911-year-oldsand10 adults.Afive-pointcalibrationprocedurewasconducted beforetheintroductoryphaseandfixationdatawere sam-pledatarateof40Hzduringstimuluspresentationinthe thresholdestimationphase
2.5 Generalprocedure TheprocedurewasapprovedbytheInstituteof Edu-cation’s Faculty Research Ethics Committee All adult participantsand parentsofchild participantsgavetheir informed consent.Childrenprovided verbalassent Par-ticipantswereseenindividuallyfortwo sessionslasting approximately 25min, each consisting of one equiva-lent noiseand onemotioncoherencetask.Theorder of presentation of conditions was counterbalanced across participants Participants were seated in a dimly lit
binocularly using a chin-rest They were instructed to maintain central fixation throughout stimulus presen-tation, which the experimenter monitored, providing reminders to maintain fixation and only initiating tri-als when the participant was attending Participants were each given a ‘Submarine Log Book’ with which they recorded their progress through the experimental session
Trang 62.6 Dataanalysis
2.6.1 Equivalentnoiseanalysis
Theequivalentnoisemodeldescribeschangesin
direc-tion discrimination threshold as a function of external
noise:
2
2
ext
where2
obsistheobserver’sthreshold,2
intisadditive inter-nalnoise,2
extistheexternalnoiseaddedtothestimulus,
andnsampistheeffectivenumberofsamplesusedto
cal-culatethemeandirectionofthestimulus.Thisapproach
exploitsadditivityofvariance,wherebyinternalnoiseand
externalnoisecontributeindependentlytoanobserver’s
directiondiscriminationthreshold
Theequivalentnoisetaskyieldedtwo thresholds:(a)
thefinestdirectiondiscriminationpossiblewithno
stim-ulus noise (‘no noise’ condition), and (b) the maximum
levelofnoisethatcouldbetoleratedwhilst
discriminat-ingalargesignaloffsetof45◦ (‘highnoise’condition).By
running Monte Carlosimulations of a model observer’s
performance acrossa rangeofinternalnoise and
samp-linglevels, Bexet al.have shown that – assumingthat
a participant’s internal noise is negligibleat high noise
levels–sampling(nsamp)canbeestimatedfromalinear
transformationoftheirmaximumtolerablenoisethreshold
(MTN):
nsamp=exp(0.000121∗MTN2+0.0357∗MTN−1.8093)
(2)
Asperformanceatlowlevelsofexternalnoiseis
deter-minedbothbyinternalnoiseandsampling,itispossibleto
usetheestimateofnsamptocomputethelevelofinternal
noise,byrearrangingEq.(1).Thus,whenexternalnoiseis
zero(2
2
Thisapproachassumesthatobservers donotchange
theirsampling(ormoregenerally,theirstrategy)asa
func-tionofexternalnoiselevel.Consistentwiththisview,the
equivalentnoisefunctionhasbeenshowntofitdirection
discriminationdataover awide range ofexternal noise
levels(directionalvariability),undervaryingstimulus
con-ditions(Dakinetal.,2005).Notethatthisapproachdoes
notassumethatobservers arenecessarilyaveragingdot
directionsinthewaythemodeldoestomakeperceptual
judgements.Nomatterhowobserversperformthetaskthe
modelwillreturntheeffectivenumberofsamplesthatare
averaged–thatistosaythattheobserverisactingasifthey
wereaveragingacertainnumberofdots.Thusallnoiseand
samplingestimatesquotedarenecessarilyeffectivevalues
sincewecannotknowtheobserver’sunderlyingstrategy
forperformingthetask
2.6.2 Datascreeningandtransformation
Alapseratewascalculatedastheproportionof
incor-rect responses to catch trials for each participant for
each condition for each task A binomial test revealed
thatparticipantsrespondingincorrectlyon4ormoreof thecatchtrials werenotperformingsignificantly above chance.Threefive-year-oldswerethereforeexcludedfrom analyses(seeSection2.1)
Analysisofvariance(ANOVA)showedthatlapserates differed significantly across age groups, F(4,118)=9.26,
p<.01,2
p=.24(5-year-olds:M=.04,SD=.06;7-year-olds:
M=.02; SD=.04, 9-year-olds: M=.01, SD=.03; 11-year-olds:M=.01, SD=.03;adults, M<.01, SD=.01).Post hoc Dunnettt-testscomparingeachoftheagegroupswiththe adultgroupsrevealedthat5-year-oldsand7-year-oldshad significantlyhigherlapseratesthanadults (5-year-olds:
p<.01;7-year-olds:p<.01),whereasthe9-and 11-year-oldsdidnot differfrom theadultgroup(p>.05).There wasnomaineffectoftask(p=.45),althoughhigherlapse rateswerefoundfortheslowspeedconditions(M=.02,
SD=.05)thanthefastspeedconditions(M=.01,SD=.03), F(1,118)=15.40,p<.01,2
p=.12.Nointeractionswere sig-nificant(ps>.05)
Toensurethatanyage-relatedand/orspeed-related dif-ferencesininternalnoise,samplingormotioncoherence thresholdswerenotaby-productofdifferencesin atten-tion,anidealobservermodelwasrunassumingdifferent levelsoflapserate.MonteCarlosimulationsallowedusto modeltheeffectofdifferinglapseratesonthresholds.We averagedacrosstaskstogetalapserateforeachobserverin eachspeedcondition,andthencorrectedthethresholdsfor eachobserveraccordingtotheirlapserateforeachspeed condition,basedonthesimulationresults
Next,theinternalnoise,samplingandmotion coher-encethreshold estimates in each speed condition were assessedforskewnessandkurtosis.Allmeasuresshowed significantpositiveskew(ps<.05)andthemajorityshowed significantkurtosis(ps<.05).Consequently,alldatawere log-transformed.Thedatawerethenscreenedforoutliers lyingmorethanthreezscoresfromthemeanforeachage groupineachspeedcondition.Nooutlierswerefoundin motioncoherencethresholds,internalnoiseorsampling estimates.Alloftheanalysesreportedbelowwere con-ductedwithlog-transformed,lapse-correctedvalues 2.6.3 Fixationanalysis
Rawfixationdatawere(x,y)coordinatessampledduring stimuluspresentationineachtrialofthethreshold estima-tionphaseforleftandrighteyepositionsrelativetothe screen’sactivedisplayarea.Thedatawereinitiallyfiltered accordingtoavaliditycodefrom0(signifyingtheeyewas definitelyfound)to4(signifyingtheeyewasnotfound) Allsampleswithvaliditycodes of2orhigherwere dis-carded(TobiiTechnology,2013).The(x,y)coordinateswere thenaveragedacrosstheleftandrighteyeforanalysis.A measureoffixationstabilitywasderivedbypoolingthe standarddeviationsoffixationlocationsinxandy dimen-sions.Thestandarddeviationswerethenlog-transformed
tominimisetheeffectsofskewnessandkurtosis
3.1 Age-relatedchangesininternalnoise Levelsofinternalnoisereducedwithage,with 5-year-oldshavingmeanlevelsof9.62◦and9.69◦intheslowand
Trang 7Fig 3. Individual values for internal noise (A), sampling (B) and motion coherence thresholds (C) for slow (1.5◦/s) (open red circles) and fast (6◦/s) (filled blue circles) conditions as a function of age Red dashed and blue solid lines represent the line of best fit for the slow and fast conditions, respectively (For interpretation of the references to color in this figure legend, the reader is referred to the web version of the article.)
Trang 8fastconditions,respectively,whichreducedto6.72◦ and
4.80◦intheadultgroup.Tocharacterisetherateof
devel-opmentalchangesinestimatedinternalnoise,loginternal
noise values wereplotted asa function of logage and
fit witha straight line(Fig.3A).Wethen comparedthe
developmentaltrajectoriesforslowandfastspeedsusing
theANCOVAmethodoutlinedbyThomasetal.(2009).In
thismethod,within-subjectseffectsareinitiallyexamined
usinganANOVAbeforeassessingage-relatedchangesby
addingacovariate(aswithin-subjectseffectsaremasked
whenabetween-subjectscovariateisadded;Delaneyand
Maxwell,1981; Thomas et al., 2009) AninitialANOVA
withspeedcondition(slow,fast)asawithin-subjectsfactor
revealedthatsignificantlyhigherlevelsofloginternalnoise
werefoundintheslow(M=.87,SD=.24)thanthefast
con-dition(M=.79,SD=.25),F(1,122)=12.24,p<.01,2
Next,anANCOVAwasconductedbyaddinglogageintothe
modelasacovariate.Overall,loginternalnoisereduced
sig-nificantlywithage,F(1,121)=13.42,p<.01,2
p=.10.Also, there wasasignificantinteractionbetweenlogageand
speedcondition,F(1,121)=4.76,p=.03,2
p=.04, indicat-ingasignificantlysteeperrateofdevelopmentinthefast
conditionthantheslowcondition
Dunnett t-tests (corrected for multiplecomparisons)
wereconductedtodeterminewhenadult-likelevelsoflog
internalnoisewerereachedforslowandfastspeed
condi-tions.Intheslowcondition,5-year-oldshadsignificantly
higherloginternalnoisethanadults(p=.02)whereas7-,
9- and11-year-oldshad adult-likelevelsofloginternal
noise(ps>.05)(5-year-olds:M=.98,SD=.25;7-year-olds:
M=.86, SD=.27; 9-year-olds: M=.87, SD=.23;
11-year-olds:M=.83,SD=.22;adults:M=.83,SD=.23).Similarly,
inthefastcondition,5-year-oldshadhigherloginternal
noisethanadults(p<.01)whereastheolderagegroupsdid
not (ps>.05)(5-year-olds: M=.99, SD=.28; 7-year-olds:
M=.78, SD=.23; 9-year-olds: M=.80, SD=.20;
11-year-olds:M=.78;SD=.21;adults:M=.68,SD=.26)
3.2 Age-relatedchangesinsampling
Next,weinvestigatedage-relatedchangesinsampling
AsshowninFig.3B,samplingincreasedfrom0.51atage
5to1.47inadultsin theslowcondition,andfrom0.98
to1.85inthefastcondition.WerepeatedtheANOVAand
ANCOVAanalysesusinglog-transformedlevelsofsampling
asthedependentvariable.Higherlevelsoflogsampling
wereobtainedinthefastcondition(M=−.06;SD=.34)than
intheslowcondition(M=.13;SD=.34),F(1,122)=39.12,
p<.01,2
p=.24.Whenlogagewasaddedintothemodel
asa covariate,it wasfoundthatlogsamplingincreased
acrossdevelopment,F(1,121)=23.32,p<.01,2
predicted However, there was no interaction between
speed conditionandlogage,F(1,121)=1.88,p=.17,
sug-gesting a similar rate of development in slow and fast
conditions
Dunnettt-testsrevealedthatallchildgroupshadlower
logsamplingcomparedtoadults(M=.17,SD=.35)inthe
slowcondition(5-year-olds:M=−.29,SD=.28;p<.01;
7-year-olds:M=−.06,SD=.35;p<.01;9-year-olds:M=−.15,
SD=.28;p<.01;11-year-olds:M=−.06,SD=.28;p=.01)
Inthefastcondition,5-year-olds(M=−.01,SD=.28)and
7-year-olds (M=−.01; SD=.25) had lower log sampling thanadults(M=.27;SD=.40)(ps<.01)whereas9-year-olds (M=.14,SD=.33)and 11-year-olds(M=.23,SD=.30)did notdiffersignificantlyfromadults(ps>.05)
3.3 Age-relatedchangesinmotioncoherencethresholds Whereas5-year-oldsrequired,onaverage,47% coher-ent motion in both the slow and fast conditions to reliably report the directionof motion, adults required only 34% and 26% coherent motion in the slow and fast conditions, respectively The ANOVA and ANCOVA analyses were repeated to characterise developmental changes in log motion coherence thresholds (Fig 3C) Higher logmotioncoherence thresholdswere foundin theslowcondition(M=−.41,SD=.16)thanthefast con-dition(M=−.51,SD=.21),F(1,122)=37.18,p<.01,2
Thresholdsdecreasedwithlogage,F(1,121)=20.50,p<.01,
2
p=.14,buttherewasnosignificantinteractionbetween speedconditionandlogage,F(1,121)=2.73,p=.10, indi-catingthatsensitivitydevelopedatasimilarrateforslow andfastspeeds
Five-year-oldsand7-year-oldshadsignificantlyhigher log thresholds than adults in both the slow and fast conditions(ps<.01),whereas9-and11-year-oldsshowed adult-like levels of performance (ps>.05) (5-year-olds:
Mslow=−.33,SDslow=.18,Mfast=−.32,SDfast=.17; 7-year-olds: Mslow=−.35, SDslow=.14, Mfast=−.44, SDfast=.17; 9-year-olds: Mslow=−.42, SDslow=.15, Mfast=−.58,
SDfast=.22; 11-year-olds: Mslow=−.48, SDslow=.14,
Mfast=−.63,SDfast=.16;adults:Mslow=−.47,SDslow=.16,
Mfast=−.58,SDfast=.17)
3.4 Relationshipbetweenequivalentnoisemeasuresand motioncoherencethresholds
Our results show that internal noise reduces, and samplingincreases,throughdevelopment,whilemotion coherencethresholdsdecrease.Nextwesoughtto inves-tigatewhetherincreasingsensitivitytocoherentmotion
is driven either by internal noise or sampling, or a combinationofboth.Correlationanalysesincludingall par-ticipantsrevealednorelationshipbetweeninternalnoise and motioncoherencethresholdsin eitherslow, r=.03,
df=122,p=.77,orfast,r=.08,df=122,p=.36,conditions However,samplingwasnegativelycorrelatedwithmotion coherencethresholdsinbothslow,r=−.35,df=122,p<.01, andfast,r=−.34,df=122,p<.01,conditions
Webuiltahierarchicalregressionmodelonlogmotion coherencethresholdsforeachspeedcondition,withlogage addedintothemodelfirst,followedbysamplingand inter-nalnoiseaddedinastepwisemanner(seeTable1).Inboth slowand fastconditions,logagesignificantly predicted motioncoherencethresholdsinthefirststepofthemodel Whensamplingandinternalnoisewereaddedintothe sec-ondstepofthemodel,ageremainedasignificantpredictor
ofmotioncoherencethresholds,andsamplingwasalsoa significantpredictorinbothslowandfastconditions Inter-nalnoise,however,failedtosignificantlypredictcoherence thresholdsforeitherspeedcondition(slow,ˇ=.14,p=.16,
orfast,ˇ=.08,p=.41),andwasthereforeexcludedfrom
Trang 9Table 1
Hierarchical regression analyses on log motion coherence thresholds in
the slow (1.5 ◦ /s) and fast (6 ◦ /s) conditions.
Step 1
Step 2
Log age −0.12 0.06 −.18 * −0.24 0.07 −.29 **
Log sampling −0.13 0.04 −.28 ** −0.16 0.05 −.26 **
Note:
In the slow condition, R 2 = 09, p < 01 for Step 1; R 2 = 06, p < 01 for Step
2 In the fast condition, R 2 = 13, p < 01 for Step 1; R 2 = 06, p < 01 for Step
2.
* p < 05.
** p < 01.
themodelinbothspeedconditions.Step2ofthemodel,
withbothlogageandsampling,wasasignificantlybetter
model than Step 1 of the model in both speed
condi-tions(seeTable1).Theresultingmodelwithlogageand
logsamplingsignificantlypredictedlogmotioncoherence
thresholdsinbothslow(F(2,120)=10.63,p<.01)andfast
(F(2,120)=14.32,p<.01)conditions
3.5 Fixationanalysis
Next,weinvestigatedwhethertherewereage-related
changesin theabilitytomaintainfixationand whether
thesewererelatedtotaskperformance.Thestandard
devi-ationofparticipants’eyepositionsforeachtaskisshown
inFig.4.ApreliminaryANOVAonstandarddeviationsin
theequivalentnoisetaskrevealednomaineffectofnoise
condition(‘nonoise’,‘highnoise’)andnointeractionswith
agegrouporspeedcondition,andsothisfactorwasnot analysedfurther
AmixedANOVAwasconductedonthestandard devi-ationswithspeed(1.5◦/s,6◦/s)andtask(equivalentnoise, motioncoherence)aswithin-participantsfactorsandage group(5-,7-,9-and11-year-oldsandadults)asa between-participantsfactor.Therewasnomaineffectofstimulus speed, F(1,54)=1.34, p=.25 However, higher standard deviations(i.e.,reducedstability)werefoundinthe equiv-alent noise task (M=−1.08, SD=.28) than the motion coherencetask(M=−1.22,SD=.28),F(1,54)=52.47,p<.01,
2
p=.49 There was a significant main effect of age, F(4,54)=4.08, p<.01, 2
p=.23 Dunnett t-tests revealed that 5-year-oldshadsignificantly largerstandard devia-tions(M=−.92,SD=.27)thanadults(M=−1.27,SD=.28),
p<.01,whereastheolderagegroupswerenotsignificantly differenttoadults(7-year-olds:M=−1.14,SD=.27; 9-year-olds:M=−1.26,SD=.26;11-year-olds:M=−1.19,SD=.23;
ps>.05).Nosignificantinteractionswerefoundbetween task,speedconditionandgroup(ps>.05)
Havingfoundthattheyoungestchildrenhavelessstable fixations than older participants, we sought to investi-gate whetherthesedifferencesrelated tointernal noise and sampling.Giventhathigher levelsofinternal noise andlowersamplingarefoundintheslowcondition (Sec-tions3.1and3.2),weconductedseparateanalysesforeach speedcondition.Intheslowcondition,fixationstandard deviationwasrelatedtointernalnoiseestimates,r=.28,
df=58,p=.04,withlowerfixationstandarddeviations(i.e., morestablefixations)beingassociatedwithlower inter-nalnoise Therewas,however,norelationshipbetween fixationstandarddeviationandsampling,r=−.14,df=58,
p=.29.Similarly, inthefastcondition,fixation standard deviation was related to internal noise, r=.30, df=58,
p=.02,butnotsampling,r=−.05,df=58,p=.72.Finally,we investigatedtherelationshipbetweenfixationstabilityand
Fig 4.Standard deviations of eye positions in equivalent noise tasks (left panel) and motion coherence tasks (right panel) for slow (1.5◦/s) and fast (6◦/s) speed conditions Circles show individual performance (slow: open circles; fast: filled circles) and lines represent mean performance for each age group (slow: red dotted line; fast: blue solid line) Standard deviations were log-transformed for analysis (For interpretation of the references to color in this
Trang 10thresh-oldswerenotrelatedtostandarddeviationofeyepositions
ineitherslow,r=.14,df=58,p=.31,orfast,r=.17,df=58,
p=.20,conditions
Thisstudypresentedanequivalentnoisemotion
inte-grationtaskalongsideatraditionalmotioncoherencetask
tochildrenaged5,7,9and11years andadultsfortwo
speed conditions (slow: 1.5◦/s; fast: 6◦/s) Thismethod
allowed us to characteriseboth age-related changes in
internal noise and sampling and the mechanisms
sup-porting coherent motion processing While there was
considerableindividual variability, wefound that
inter-nalnoiseestimatesreducethroughchildhood,reflecting
improvedlocalprocessing,andthat thisisaccompanied
byanincreaseinthenumberofsamplesthechildcanuse
toestimateglobalmotion.Notethattheeffectivenumber
ofsamplescanalsobethoughtofasameasureof
multi-plicativenoisebeingaddedtoallestimatesinthepooling
process(i.e.,‘globalnoise’;Dakinetal.,2005).Although
levelsofinternalnoisereducedwithage,thesedidnot
pre-dictmotioncoherencethresholds.Instead,developmental
increases in motioncoherence sensitivity appear to be
drivensolelybyage-relatedincreasesinsampling
Overall,higherlevelsofinternalnoiseandlower
samp-lingwere foundin theslow(1.5◦/s)condition thanthe
fast(6◦/s)condition,whichmightreflectdistinct
speed-tunedmotionprocessingsystems (e.g.,Thompsonetal.,
2006).Generallypoorer performancemight bea
conse-quenceoffewerneuronstunedtoslowspeedsthanfast
speeds,asfoundintheprimatebrain(Hadadetal.,2011;
LiuandNewsome,2003).Wewereparticularlyinterested,
however, in how internal noise and sampling changed
withage,and how theseage-relatedeffects might vary
betweenspeed conditions.Internalnoise levelsreduced
more gradually in the slow (1.5◦/s) condition than the
fast(6◦/s)condition,whereassamplingfollowedasimilar
rate of developmentfor slow and faststimuli
Further-more,samplingappearedtofollowamoreprotractedrate
ofdevelopmentthanthatofinternalnoise.Internalnoise
reachedadult-likelevelsbyapproximately7yearsofage,
while sampling reachedadult-likelevels at a later age
Indeed,samplingwasadult-likeby9yearsinthefast
con-dition,butwasnotyetadult-likeby11yearsintheslow
condition
OurresultscomplementarecentstudybyBogfjellmo
et al (2014),which found increasedsamplingof
direc-tioninformationbetweentheagesof6and17yearsfor
stimulusspeedsof2.8◦/sand9.8◦/s,whilelevelsof
inter-nal noise remained stable Taken together, the current
resultsandthoseofBogfjellmoetal.suggestthat
inter-nal noise reducesto adult-like levelsby approximately
6–7years, whileage-relatedchangesinsamplingfollow
amoreextendedtrajectory.Ourfindingthatinternalnoise
reduceswithageechoesapreviousstudyintheauditory
domainwhichreportedhigherinternalnoiseinchildren
aged 6–11yearscompared toadults(Bussetal., 2006),
aswellasreportsofincreasedlevelsofinternalnoisein
infants(SkoczenskiandNorcia,1998)
Theequivalentnoisemethodgivesusanestimateofthe totalamountofinternalnoise,whilstremainingagnostic aboutitsprecisesource.However,wespeculatethathigh levelsofinternalnoiseinourdirectionintegrationtaskmay reflectimmaturityintheresponsesofdirection-sensitive cellsinV1.Specifically,imprecisioninestimatingthe direc-tionsoflocalelementsmaybeduetobroadbandwidthsof V1neuronsinchildrenbelowtheageof7years,whichlater narrowwithdevelopment(atleastintheprimatebrain,
Hatta etal.,1998).Conversely,developmental increases
insamplingmay reflectthe developmentofneuronsin higherareasofthemotionprocessinghierarchythought
tobeinvolvedinintegratinglocalmotionsignals,suchas MT/V5(BornandTootell,1992;Brittenetal.,1992).While
MTneuronsareresponsivetodirectioninformationand myelinatedatbirthinprimates(Flechsig,1901;Movshon
etal.,2004),theyshowimmaturitiesintheirintegrative properties(Movshonetal.,2004),whichcouldunderliethe extendeddevelopmentofsamplingreportedhere Further-more,thefactthatinternalnoisematuresbeforesampling corroboratesneurophysiologicalresearchshowingthatV1 maturesearlierthanextrastriateareas(Distleretal.,1996;
Gogtayetal.,2004;Houetal.,2009;Kourtzietal.,2006), whichhasbeenlinkedtodifferencesinsynapticpruning (Distleretal.,1996;Gogtayetal.,2004).Futurework com-biningpsychophysicalandneurophysiologicalmeasuresis necessaryto determinethepreciseneural substratefor theseeffects
Ourfindingsofage-relatedreductionsininternalnoise contrastsharplywithMcIntosh etal.’s (2008)reportof increasingneuralnoisemeasuredbyintra-participantEEG variabilitybetweentheagesof8and12years.McIntosh
etal.suggestedthatincreasingneuralnoisereflectedthe brain’s increasingcomplexity withage,allowingone to exploremultiplestatesandadapttodifferentsituations Thissortofcomplexity,however,isnotbeingtappedbythe visualintegrationtaskusedhere,andinstead,wereferto internalnoiseasuncertaintyinthecodingoflocalmotion directions Indeed, there are many different sources of noisewithinthenervoussystem(Faisaletal.,2008)andit
ispossiblethatnoisemayhavedifferenteffectsatdifferent levelsofthecorticalhierarchy.However,current compu-tationalandneuralmodelsofnoisearebasedonanimal andhumanadultbrains.Itthereforeremainsachallengeto determineexactlyhowthesemodelsshouldbeappliedto thedevelopingbrain.Thediscrepancybetweenourresults andthoseofMcIntoshetal.highlighttheimportanceof specifyingwhatismeantbynoiseandthelevelatwhich
itisthoughttohaveaneffectwhenconstructing develop-mentalmodels
Ourfindingsaddtoabodyofliteratureshowinga rel-ativelyprotracteddevelopmentofsensitivitytocoherent motion(Gunnetal.,2002;Hadadetal.,2011).Ourresults suggestthatmotioncoherencethresholdsreachadult-like levelsbyapproximately9years,whichisslightlyearlier thanpreviousaccountsthathavesuggestedthatmaturityis reachedby10–11yearsofage(Gunnetal.,2002),or12–14 yearsofage(Hadadetal.,2011).Discrepanciesintheageat whichadult-likelevelsarereachedarelikelytobedueto differencesinarangeofstimulusparameters(Narasimhan andGiaschi,2012).Ourstudyalsoallowedustotestthe